<Original Articles>

Analysis of factors affecting crestal bone loss around the implants

Ji-Hoon Park1, Young-Kyun Kim1, Pil-Young Yun1, Yang-Jin Yi2, In-sung Yeo2, Hyo-Jung Lee3, and Jin-Young Park2

1. Dept. of Oral and Maxillofacial Surgery, 2. Dept. of Prosthodontics, 3. Dept. of Periodontology, Dentistry Section, Seoul National University Bundang Hospital

Corresponding Author
Young-Kyun Kim, DDS, PhD Department of Oral and Maxillofacial Surgery, Dentistry Section 300 Gumidong, Bundang-gu, Seongnam City, Gyundgi-do, Korea Tel : 82-31-787-7541 Fax : 82-31-787-4068 E-mail : kyk0505@freechal.com
Received for publication Aug 17, 2009; received after revision Sep 9, 2009; Accepted for publication Sep 28, 2009

Abstract
Purpose : To determine whether peri-implant crestal bone loss could be affected by systemic disease, primary ISQ value, implantation method (submerged vs. non-submerged), surface treatment, and bone density Materials and methods : Patients who underwent fixture installation from June 24, 2005 to October 23, 2008 at Seoul National University Bundang Hospital were evaluated. A total of 157 patients (male: 52, female: 85) had 346 fixtures installed. Among them, 49 patients had periapical radiographs taken 1 year after prostheses were first set. A total of 97 fixtures were implanted. In particular, 30 fixtures were installed in patients with systemic diseases such as diabetes mellitus, cardiovascular disease, hypertension, and liver disease. The immediate stability of implants was measured with Osstelltm. Implant surface treatment was classified into two groups (RBM, Cellnest (Anodized)), and bone density, into four groups (D1~D4). The bone resorption on the mesial and distal areas of fixtures was measured with periapical radiographs using the paralleling technique, and the mean value was calculated. The length determination program in IMPAX (AGFA, Belgium) was used. Results : At least 332 out of 346 (96%) installed GS implants were successfully osseointegrated 1 year after prostheses were first set. The mean value of the bone resorption of the installed GS implants was 0.44mm. The minimum value was 0mm, and the maximum value, 2.85mm. There was a statistically significant difference between the implantation methods (submerged, non-submerged) with regard to the amount of alveolar bone loss 1 year after prostheses were first set (p<0.05). Non-submerged implants showed less crestal bone loss. Note, however, that other variables had no correlation with crestal bone loss (p>0.05). Conclusion : There was a statistically significant difference between the 1-stage method and 2-stage method with regard to the amount of alveolar bone loss 1 year after prostheses were first set. Systemic disease, primary ISQ value, surface treatment, and bone density were not associated with alveolar bone loss. Other variables were assumed to have a correlation with alveolar bone loss.
Keywords : crestal bone loss, implant J Kor Dent Sci. 2009; 3(1) : -

12 I

J Kor Dent Sci.

Analysis of factors affecting crestal bone loss around the implants

Introduction
Upon placement, an implant has to be maintained in stable state without external force for a fixed period of time to allow the peripheral osteocyte and veins to form the bone and integrate with the surface of the implant. Prosthetic restoration takes place after successful osseointegration; resorption will proceed gradually over time after the prostheses begin to function. In 1986, Albrektsson, et al, suggested the standard for successful implant, i.e., 1.5mm or less bone loss in the first year after implant placement and 0.2mm or less vertical bone loss a year later1). There are many elements that can accelerate the resorption of alveolar bone, and they can be categorized into systemic factors such as whether the patient has systemic disease and local factors such as surface treatment of implant, obesity, and inflammation around the implant. The initial failure of implant is generally accepted to be caused mainly by the failure of close contact between bone and implant. Likewise, both systemic factors and local factors can interrupt primary cell reaction2,3). On the other hand, the post-failure of implant and bone resorption are related to overload or inflammation around the implant due to microbial infection4). The primary placement of implant can be divided into onestage surgery and two-stage surgery. In the past, it was considered natural that the top area of the implant be covered with soft tissue during osseointegration to minimize the infection, the apical proliferation of the epithelium. So two-stage surgery was general. Symptoms such as infection, mobility, and resorption were considered to have been caused by the exposure of the implant inside the oral cavity. Note, however, that recent studies reported no large difference between one-stage surgery and two-stage surgery5-9). This study performed a comparative analysis on bone resorption 1 year after prostheses placement for Osstem GS (Osstem, Korea) Implant to examine the post-resorption of bones around the implant and correlations between a number of elements.

patients (72 males, 85 females), and a total of 346 implants were placed. At least 49 patients had periapical radiograph 1 year after prostheses placement (28 males, 21 females), with a total of 97 implants placed. The survey on the survival rate targeted all patients, and the resorption of the alveolar bone was measured for patients whose periapical radiograph remained 1 year after prostheses placement. A total of 30 implants were placed in patients with systemic disease. Diseases were classified into diabetes, cardiovascular disease, high blood pressure, and liver disease. The initial stability during placement was measured with Osstell MentorTM and was categorized into 10 steps from the minimum value of 30. Surface treatment was divided into two categories: RBM and CellNest (Anodized). Bone substance was measured based on the feel of the surgeon and categorized into D1~D4. A total of 62 implants were placed in 1-stage surgery (non-submerged), and at least 35 implants, in two-stage surgery (submerged). To measure bone resorption, the distance between the first screw thread to the very top of the resorbed alveolar crest as represented in the parallel periapical radiograph was measured; alveolar bone resorption on the mesial and distal sides was measured with the distance measurement program of IMPAX (Agfa, Belgium), with the average recorded (Fig. 1). SPSS 12.O (LEAD Technology, USA) was used for statistical calculation. The Kruskal-Wallis method was used to measure change in bone resorption due to systemic disease and initial stability, and the Mann-Whitney method, to measure change in bone resorption due to surface treatment. Independent T-test was utilized to measure the difference between one-stage surgery and two-stage surgery,

Materials and Methods

Patients who went through the Osstem GS Implant (Osstem, Korea) placement surgery from June 2005 to October 2008 were surveyed. There were a total of 157

Fig 1. Method of measuring crestal bone loss. On the mesial and distal sides, the resorption volume of the implant fixture top and the first bone contact area was measured. The average was then calculated.
Ji-Hoon Park et al : Analysis of factors affecting crestal bone loss around the implants. J Kor Dent Sci 2009.

Vol 3, No 1 2009.

I 13

Table 1. Systemic disease and crestal bone loss (Kruskal-Wallis) (p = 0.263) Systemic Disease n Bone Loss (mm) .42 0 .32 .62 1.58 S.D. .53 0 .31 .84 1.80

Table 2. ISQ value (measured at 1st surgery) and crestal bone loss (Kruskal?Wallis) (P = 0.122) ISQ (1st surgery) 30~39 40~49 50~59 60~69 70~79 80~89 n 6 4 9 26 32 18 Bone Loss (mm) .43 1.28 .49 .49 .43 .23 S.D. .74 1.08 .49 .58 .60 .26

None 67 Liver disease 2 Cardiovascular disease 16 Diabetes mellitus 10 Hypertension 2

Ji-Hoon Park et al : Analysis of factors affecting crestal bone loss around the implants. J Kor Dent Sci 2009.

with the statistical significance of the difference in bone resorption due to the change in bone substance verified through ANOVA. Note, however, that the post-hoc test was not performed since it did not have statistical significance. The test was considered to have statistical significance in case the P value was smaller than 0.05.

Ji-Hoon Park et al : Analysis of factors affecting crestal bone loss around the implants. J Kor Dent Sci 2009.

Results
At least 332 out of the 346 GS implants (96%) placed survived 1 year after prostheses placement. Alveolar bone resorption was measured to be a minimum of 0mm to a maximum of 2.85mm and 0.44mm on the average 1 year after prostheses placement. There was no significant difference in bone resorption between systemic patient groups. Patients without any disease (n=67) showed 0.42mm (s.d.=0.53) of bone resorption on the average, whereas patients with liver disease (n=2) recorded 0mm. Patients with cardiovascular

Table 3. Surface treatment and crestal bone loss (Mann-Whitney) (P = 0.555) Surface Treatment RBM Anodized (Cellnest) n 87 8 Bone Loss (mm) .46 .31 S.D. .60 .37

disease (n=16) exhibited 0.32mm (s.d.=0.31) of bone resorption, diabetics (n=10) recorded 0.62mm (s.d.=0.84), and hypertensives (n=2) showed 1.58mm (s.d.=1.80). Hypertensives showed a relatively large difference compared to other groups, but such was not statistically significant due to the small number of patients (p = 0.263). (Table 1) ISQ during placement was categorized into 30~39(n=6), 40~49(n=4), 50~59(n=9), 60~69(n=26), 70~79(n=32), and 80~89(n=18); resorption decreased when ISQ increased excluding the 30~39 sections, but the difference was not statistically significant (p value = 0.122). (Table 2) Bone resorption due to implant surface treatment did not show any statistically significant difference 1 year after prostheses placement (p value = 0.555). (Table 3) Bone resorption due to the difference in placement method (one-stage surgery, two-stage surgery) showed a statistically significant difference 1 year after prostheses placement, with the one-stage surgery exhibiting less resorption (p value = 0.016). (Table 4) Bone resorption due to the difference in bone substance as felt by the surgeon 1 year after prostheses placement did now show any statistically significant difference (p value = 0.636). (Table 5)

Ji-Hoon Park et al : Analysis of factors affecting crestal bone loss around the implants. J Kor Dent Sci 2009.

Table 5. Bone density and crestal bone loss (ANOVA) (P-value = 0.636) Table 4. Implantation method and crestal bone loss (T-test) (P = 0.016*) Implantation Method 1-stage 2-stage n 35 62 Bone Loss (mm) .28 .53 S.D. .28 .69 Bone Quality D1 D2 D3 D4 n 12 28 24 33 Bone Loss (mm) .25 .45 .43 .51 S.D. .33 .58 .64 .63

Ji-Hoon Park et al : Analysis of factors affecting crestal bone loss around the implants. J Kor Dent Sci 2009.

Ji-Hoon Park et al : Analysis of factors affecting crestal bone loss around the implants. J Kor Dent Sci 2009.

14 I

J Kor Dent Sci.

Analysis of factors affecting crestal bone loss around the implants

Discussion
Bone resorption is known to take place mainly during the first year after prosthesis placement, decreasing considerably after the prosthesis is stabilized10). There is no precise known cause for initial bone resorption around the implant, but some studies suggested that it could be caused by the interruption of blood circulation due to the external injury made during surgery11, 12). Moreover, some studies cited other possible causes such as overload, biological width, and crest module13). Other studies reported that bone resorption around the implant was caused by the gap between the implant and the abutment14) and suggested a technique such as platform switching based on the study results. Bone loss within the first year of placement of the top prosthesis can be caused by the combination of local or systemic factors, although the cause is not precisely known in many cases. In this study, whether or not the patient had systemic disease did not appear to have influenced bone resorption 1 year after prosthesis placement. Other studies that examined the relationship between systemic diseases and implant success rate and bone resorption found statistically significant difference in the rate of occurrence of complications between patients with systemic disease and healthy patients and reported that the rate of occurrence of complications was especially high in hypertension, cerebrovascular disease, and psychiatric disease groups. Note, however, that there was no significant difference in bone resorption 1, 2, or 3 years after the surgery between patients with systemic disease and healthy patients15). There was no study that examined the relationship between cardiovascular disease and implant failure16). Moy, et al reported that implant placement was not a clear contraindication for patients with cardiovascular disease17). For cerebrovascular disease, the person is only considered a patient 6~12 months after the initial treatment period; the patient should not receive any stress including surgical operations within 3~6 months of the stabilization period. Otherwise, ischemic complications may occur. Furthermore, some studies reported that the normal removal of implant was closely related to the mental factor, although there were no biological evidences supporting the finding that more implant failures are found in mental patients. OsstellTM is used to measure the stability of the implant; it is called resonance frequency analyzer. As the principle of

operating this device, it applies vibration to the boneimplant interface and measures the rebound. The measured value is called ISQ (implant stability quotient). When the interface grows, ISQ decreases18). The initial stability did not have a significant relationship with bone resorption 1 year after prosthesis placement, but bone resorption appeared to be less given higher initial ISQ excluding the ISQ 30~39 sections. The surface treatment of the implant is known to have an impact on the cell reaction speed. The anodizing surface makes a porous crater-like surface structure by electrochemically anodizing the metal substrate on the titanium surface. RBM (resorbable blasting media) creates a rough surface by spraying materials that can be absorbed inside the body such as HA (Hydroxyapatite: Ca10(PO4)6(OH2)) powder on to the titanium surface; it was developed to resolve the problem of aluminum oxide. Used to be applied as spray material, aluminum oxide can have a negative impact on osseointegration in case it is not completely eliminated. The study that examined the association between surface treatment and wettability reported less wettability and implant removal torque obtained given greater surface contact angle of moisture. On the other hand, better wettability and removal torque were obtained with smaller surface contact angle. Some studies reported that the anodized surface had the best wettability, and the machined surface, the worst19). Moreover, some studies reported a significant difference in bone resorption around the implant after functioning between the implant with machined surface and implant with anodized surface and claimed more bone resorption was found with the machined surface implant20). We could not find any articles that had been studied the significant difference in bone resorption between the anodized implant and RBM-treated implant. In this study, the one-stage surgery and two-stage surgery showed significant differences in crestal bone resorption, with less bone resorption observed in the one-stage surgery. Other studies that surveyed the success rate of implants did not find huge differences in the changes taking place in the peripheral bones after the application of two surgery methods21, 22); neither did they find significant differences in the resorption of alveolar crestal bone 23). The implant placement is divided into the one-stage surgery and twostage surgery according to exposure. One-stage surgery is popularly applied since it does not require additional

Vol 3, No 1 2009.

I 15

surgery, requiring short recovery period and having little difference in the success rate compared with the two-stage surgery. Note, however that some studies claimed that onestage surgery and two-stage surgery had similar success rates, although two-stage surgery tended to show lower failure rate, more so with completely edentulous patients. Accordingly, studies recommended one-stage surgery, which involved less surgery and fast recovery for partially edentulous patients who are less affected by the additional external force, and two-stage surgery, for completely edentulous patients who are likely affected by external force or patients who did not achieve initial stability24). This study did not show significant difference in bone resorption due to the bone substance identified by the surgeon (Lekholm & Zarb, 1985) 1 year after prostheses placement. Bone quality and quantity are two important elements in establishing an appropriate treatment plan and obtaining sufficient surface contact. According to studies, the weight applied to the implant is an important element in crestal bone loss25-28); the weight on the implant can be distributed through sufficient surface contact. Some studies reported that placing an implant with a special design that allows sufficient surface contact in inferior bone substance

such as D4 will help prevent alveolar bone resorption and reduce failures29). One of the limitations of this study was that it could not standardize the variables influencing bone resorption. In other words, long-term, more systematic studies must be conducted on the elements influencing the resorption of the bone around the implant after standardizing a number of variables such as the type of surgical methods, bone graft material, type of bio-materials such as barrier membrane, type of upper prostheses, and condition of antagonist teeth.

Conclusion
This study did not find statistically significant difference in the peripheral bone resorption of the implant 1 year after prostheses placement due to the existence of systemic disease, initial fixed value, and surface treatment. Likewise, statistically significant difference in bone resorption due to the placement method (one-stage surgery, two-stage surgery) was found, with one-stage surgery showing less resorption.

References
1. Albrektsson, T., Zarb, G., Worthington, P., and Eriksson, R.A. The long-term efficacy of currently used dental implants: review and proposed criteria of success. Int. J. Oral Maxillofac Implants. 1986; 1:11~25. 2. Esposito, M., Hirsch, J.M., Lekholm, U., and Thomsen, P. Biological factors contributing to failures of osseointegrated oral implants(II). Etiopathogenesis. Eur J Oral Sci. 1988; 3:721~764. 3. Quirynen, M., De Soete, M., and van Steenverghe, D. Infectious risks for oral implants: a review of literature. Clin Oral Impl Res. 2002; 14:1~19. 4. van Steenberghe, D., Lekholm, U., and Bolender, C., et al. Applicability of osseointegrated oral implants in the rehabilitation of partial edentulism: a prospective multicenter study on 558 fixtures. Int J Oral Maxillofac Implants. 1990; 5:272~281. 5. Schroeder, A., van der Zypen, E., Stich, H., and Sutter, F. The reaction of bone, connective tissue, and epithelium to endosteal implants with sprayed titanium surfaces. J. Maxillofac. Surgery. 1981; 9:15~25. 6. Babbush, C.A., Kent, J.N., and Misiek, D.J. Titanium plasmasprayed (TPS) screw implants for the reconstruction of the edentulous mandible. J Oral Maxillofac Surg. 1986; 44:274~282. 7. Buser, D., Weber, H.P., Bragger, U., and Balsiger, C. Tissue integration of one-stage ITI implants: 3-year results of a longitudinal study with hollow cylinder and hollow screw implants. Int J Oral Maxillofac Implants. 1991; 6:405~412. 8. Weber, H.P., Buser, D., Fiorellini, J.P., and Williams, R.C. Radiographic evaluation of crestal bone levels adjacent to nonsubmerged titanium implants. Clin Oral Impl Res. 1992; 3:181~188. 9. Ericsson, I., Randow, K., Glantz, P.O., et al. Clinical and radiographic features of submerged and non-submerged titanium implants. Clin Oral Impl Res. 1994;5(3):185~9. 10. Ahlqvist, J., Borg, K., Nilson, H., et al. Osseointegrated implants in edentulous jaws: a 2-year longitudinal study. Int J Oral Maxillofac Implants. 1990; 5(2):155~62. 11. Adell, R., Lekholm, U., Rockler, B., et al. Marginal tissue reactions at osseointegrated titanium fixtures: a 3-year longitudinal prospective study. Int J Oral Maxillofac. Surg. 1986; 13:39~52. 12. Adell, R., Lekholm, U., Rockler, B., and Branemark, P.I. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg. 1981; 6:387~416. 13. Oh, T.J., Yoon, J.K., and Wang, Misch C.E. Causes of early implant bone loss: myth of science. J Periodontol. 1997; 68:186~198. 14. Herman, J.S., Cochran, D.L., Nummikoski, P.V., and Buser, D. Crestal bone changes around titanium implants: a radiographic evaluation of unloaded non-submerged and submerged implants in the canine mandible. J Periodontol. 1997;68(11):1117~1130. 15. Kim, J.H., and Kim, Y.K. Clinical study on the implant treatment in patients with systemic disease. Implantology. 2009;13(2):64~75.

16 I

J Kor Dent Sci.

Analysis of factors affecting crestal bone loss around the implants

References
16. van Steenberghe, D., Quirynen, M., Molly, L., et al. Impact of systemic diseases and medication on osseointegration. Periodontol. 2003;33:163~171. 17. Moy, P.K., Medina, D., Shetty, V., et al. Dental implant failure rates and associated risk factors. Int J Oral Maxillofac Implants. 2005;20(4):569~577. 18. Balleri, P., Cozzolino, A., Ghelli, L., et al. Stability measurements of osseointegrated implants using Osstell in partially edentulous jaws after 1 year of loading: a pilot study. Clin Implant Dent Relat Res. 2002;4:128~132. 19. Elias, C.N., Oshida, Y., Lima, J.H., and Muller, C.A. Relationship between surface properties (roughness, wettability, and morphology) of titanium and dental implant removal torque. J Mech Behav Biomed Mater. 2008; 1(3): 234~242. 20. Watzak, G., Zechner, W., Busenlechner, D., et al. Radiological and clinical follow-up of machined- and anodized-surface implants after mean functional loading for 33 months. Clin Oral Impl Res. 2006;17(6):651~7. 21. Gotfredsen, K., Rostrup, E., Hjorting-Hansen, E., et al. Histological and histomorphometrical evaluation tissue reactions adjacent to endosteal implants in monkeys. Clin Oral Impl Res. 1991;2:30~37. 22. Abrahamsson, I., Berglundh, T., Moon, I.S., and Lindhe, J. Periimplant tissues at submerged and non-submerged titanium implants. J Clin Periodontol. 1999;26(9):600~7. 23. Cecchinato, D., Olsson, C., and Lindhe, J. Submerged or nonsubmerged healing of endosseous implants to be used in the rehabilitation of partially dentate patients. J Clin Periodontol. 2004;31(4):299~308. 24. Esposito, M., Grusovin, M.G., Chew, Y.S., et al. Interventions for replacing missing teeth: 1-versus 2-stage implant placement. Cochrane Database Syst Rev. 2009;(3): CD006698. Review. 25. Quirynen, M., Naert, I., van Steenberghe, D., et al. A study of 589 consecutive implants supporting complete fixed prostheses: I. Periodontal aspects. J Prosthet Dent. 1992;68:655~663. 26. Adell, R., Eriksson, B., Lekholm, U., et al. Long-term follow-up study of osseointegrated implants in the treatment of totally edentulous jaws. Int J Oral Maxillofac Implants. 1990; 5:347~359. 27. Naert, I., Duyck, J., Hosny, M., et al. Evaluation of factors influencing the marginal bone stability around implants in the treatment of partial edentulism. Clin Implant Dent Relat Res. 2001; 3: 30~38. 28. Engquist, B., Bergendal, T., Kallus, T., et al. A retrospective multicenter evaluation of osseointegrated implants supporting overdentures. Int J Oral Maxillofac Implants. 1988; 3: 129~134. 29. Kline, R., Hoar, J.E., Beck, G.H., et al. A prospective multicenter clinical investigation of a bone quality-based dental implant system. Implant Dent. 2002; 11: 224~234.

Vol 3, No 1 2009.

I 17